Drought, fire, and rainforest endemics: A case study of two threatened frogs impacted by Australia's “Black Summer”

Abstract Deepening droughts and unprecedented wildfires are at the leading edge of climate change. Such events pose an emerging threat to species maladapted to these perturbations, with the potential for steeper declines than may be inferred from the gradual erosion of their climatic niche. This study focused on two species of amphibians—Philoria kundagungan and Philoria richmondensis (Limnodynastidae)—from the Gondwanan rainforests of eastern Australia that were extensively affected by the “Black Summer” megafires of 2019/2020 and the severe drought associated with them. We sought to assess the impact of these perturbations by quantifying the extent of habitat affected by fire, assessing patterns of occurrence and abundance of calling males post‐fire, and comparing post‐fire occurrence and abundance with that observed pre‐fire. Some 30% of potentially suitable habitat for P. kundagungan was fire affected, and 12% for P. richmondensis. Field surveys revealed persistence in some burnt rainforest; however, both species were detected at a higher proportion of unburnt sites. There was a clear negative effect of fire on the probability of site occupancy, abundance and the probability of persistence for P. kundagungan. For P. richmondensis, effects of fire were less evident due to the limited penetration of fire into core habitat; however, occupancy rates and abundance of calling males were depressed during the severe drought that prevailed just prior to the fires, with the reappearance of calling males linked to the degree of rehydration of breeding habitat post‐fire. Our results highlight the possibility that severe negative impacts of climate change for montane rainforest endemics may be felt much sooner than commonly anticipated under a scenario of gradual (decadal‐scale) changes in mean climatic conditions. Instead, the increased rate of severe stochastic events places these narrow range species at a heightened risk of extinction in the near‐term.


| INTRODUC TI ON
It is now clear that severe droughts and unprecedented wildfires are at the leading edge of climate change, and will threaten some species long before forecast erosion of their climatic niche (Kelly et al., 2020). The burgeoning risk of wildfire with the accumulation of carbon dioxide in the atmosphere has been predicted for some time (Scholze et al., 2006). Longer and more extreme fire seasons have been predicted for already fire-prone regions, resulting from increasing temperatures, more erratic rainfall, deeper droughts, and heatwaves (Hennessy et al., 2005;Moriondo et al., 2006;Pitman et al., 2007). However, intense droughts and concomitant fire events are increasingly impacting regions and ecosystems in which they were historically extremely rare or unknown, including tropical and sub-tropical rainforests in Australia, south-east Asia, and South America (Barlow et al., 2020;Chisholm et al., 2016;Collins et al., 2021).
Montane species are particularly threatened by climate change.
The typically small range and narrow climatic niche of these species leaves them inherently susceptible (Ohlemüller et al., 2008), as does their lower thermal tolerances and adaptation to moist environments (McCain & Colwell, 2011). Studies on the impacts of climate change on montane species have subsequently focused on these mechanisms, often aided by forward-projection of environmental niche models. In Australia, for example, significant effort has been expended over the last two decades building environmental niche models to estimate the scale and pace of range contractions for montane species under climate change, with focus on gradual changes to temperature and rainfall profiles (Bateman et al., 2012;Bond et al., 2011;Costion et al., 2015;Das et al., 2019;Fordham et al., 2016;Kearney et al., 2010;Sopniewski et al., 2022;Williams et al., 2003). While an important and valid approach, these studies usually exclude alteration of drought and fire regimes under climate change, at least explicitly. Recent increases in the frequency, extent, and severity of wildfire across Australia in the last two decades (Abram et al., 2021)-including megafires that have penetrated ecosystems never previously known to burn (Hines et al., 2020;Holz et al., 2015)-suggest that sharp changes in fire regimes driven by severe drought may be crucial to such projections.
The "Black Summer" megafires across eastern Australia during 2019/2020 highlighted the risk that unprecedented drought and fire poses to Australia's biodiversity under climate change (Legge et al., 2022;Rumpff et al., 2023;Ward et al., 2020). These fires burnt ~10 M hectares of woodland, forest, and rainforest during Australia's hottest and driest year on record (Collins et al., 2021;Filkov et al., 2020). The radiative power of these fires, the area burnt at high severity, and the area of rainforest burnt, were all without precedence in the historical record (Abram et al., 2021;Collins et al., 2021;Rumpff et al., 2023). In northern New South Wales and southeast Queensland, some 53% of the Gondwana Rainforests of Australia World Heritage Area was affected by fire during the 2019/2020 event (DAWE, 2020a). While the majority of these impacts occurred in fire-adapted eucalypt forest, a considerable area of fire-sensitive subtropical, warm-temperate, and cool-temperature rainforest was also burnt (DAWE, 2020a).
The Gondwanan rainforests of northern New South Wales and southern Queensland support several species of endemic, rangerestricted amphibians that contribute to the outstanding universal values of the World Heritage area. Notable among these are six of seven species in the genus Philoria (Limnodynastidae), being P. knowlesi, P. kundagungan, P. loveridgei, P. pughi, P. richmondensis, and P. sphagnicolus (Knowles et al., 2004;Mahony et al., 2022).
These species are all allopatric, occurring as scattered mountaintop endemics restricted to headwater drainage lines, seepages, and small bogs in rainforest and adjoining mesic vegetation (Knowles et al., 2004, Mahony et al., 2022. Males construct and call from nests in saturated soil. Tadpoles complete their development within the nest and their survival is dependent on constant moisture (Anstis, 2013). Microhabitat use outside the breeding season is almost totally unknown; however, radio-tracking studies on the southern member of the genus from Victoria, P. frosti, indicate that both males and females likely migrate small distances (<85 m) away from seepages post-breeding to occupy moist microhabitats slightly upslope (Hollis, 2003).
The reliance of Philoria on moist or saturated microhabitats within rainforest and adjoining mesic forest, suggests that they may be particularly sensitive to increased drought and novel fire under climate change Mahony et al., 2023;Newell, 2018).
This study sought to assess the impact of the "Black Summer" fires and the severe drought associated with them on two species from the Gondwana Rainforests of Australia World Heritage Area-P. kundagungan and P. richmondensis. Both are listed as Endangered by the International Union for the Conservation of Nature (IUCN, 2021) and the Australian Government (DCCEEW, 2022).
We had four aims for each species: (1) estimate the portion of potential habitat affected by the 2019/2020 fires; (2) resurvey all previous survey sites post-fire, adding new sites in fire-impacted catchments; (3) examine the effects of fire and drought on site occupancy probability and abundance of calling males, and; (4) assess changes in site occupancy and calling male abundance from surveys completed pre-fires, and determine the roles of drought and fire on these dynamics.

| Study area and survey sites
The study area extended across the uplands of north-eastern New South Wales and south-eastern Queensland (Figure 1). In the east, surveys were completed for P. richmondensis in Yabbra, Richmond Range and Toonumbar National Parks. In the west and north-west of the study area, surveys were completed for P. kundagungan in Tooloom and Koreelah National Parks in New South Wales, and along the length of Main Range National Park in Queensland.
Sites were defined as 100 m transects along headwater streams (1st or 2nd order) beginning from the first expression of surface water. An original set of sites for P. richmondensis (n = 37) was established in 2012 with the aid of a species distribution model (Willacy, 2014). Sites were randomly located in 12 headwater stream catchments that displayed a predicted habitat suitability of 40% or greater, under the criterion that they were at least 200 m apart and within 500 m of a road or trail. An original set of sites for P. kundagungan (n = 35) was established by Bolitho et al. (2021) in 2016. Sites were randomly selected across the range of this species under three constraints: (1) they were within 500 m of rainforest; (2) they were >500 m from another site, and; (3) they were within 2 km of a road or operational fire trail. F I G U R E 1 Map of the study area, showing locations of transects surveyed for Philoria kundagungan (a) and Philoria richmondensis (b), and their positions relative to the extent and severity of fire during the "Black Summer" wildfires of 2019/2020.

(a) (b)
To increase coverage of habitat burnt during the 2019/2020 fires, we added a further 13 sites for P. kundagungan at the northern and southern extremities of Main Range National Park, and a further 13 sites for P. richmondensis at the southern end of Yabbra National Park (the only area within the species' range that was affected by these fires). In total, 48 sites were surveyed for P. kundagungan (14 burnt) and 50 sites surveyed for P. richmondensis (13 burnt).

| Surveys
Surveys were completed for calling males between September 2020 and February 2021; the breeding season immediately following the "Black Summer" fires. Both species call primarily in the Austral spring, with a peak of calling in September-October and gradual reduction in calling as temperatures increase in summer (Bolitho et al., 2021;Willacy et al., 2015).

| Field assessments of fire severity and drought stress
Fire impacts at each site were scored using a suite of measures. and 20 m perpendicular to the stream bed was estimated for each 10 m section of the transect. This allowed the total percentage of the bank burnt on each side of the stream to be estimated for each distance class. Fire severity was also scored on an ordinal scale in each of these zones on the stream bank, as either: (1) "Unburnt"; (2) "Low" (canopy and subcanopy unscorched, shrubs may be scorched, fire-sensitive low shrubs may be killed); (3) "Moderate" (partial canopy scorch, subcanopy partially or completely scorched, and/or fire-sensitive tall shrub or small tree layer mostly killed); (4) "High" (full canopy scorch to partial canopy consumption, subcanopy fully scorched, or consumed), or; (5) "Extreme" (full canopy, subcanopy, and understorey consumption). In situations where different levels of fire severity were present in a stream bank zone, the severity category that covered the largest proportion of the burnt area of the zone was assigned. Sites burnt at varying levels of severity are depicted in Figure 2. Willacy, 2014) that is highly sensitive to desiccation. These estimates were derived using the same approach as that applied for estimating to percentage of the stream bed burnt (as above).

| Remote-sensed variables
To complement field-based measures of fire severity at each site, the Australian Google Earth Engine Burnt Area Map (GEEBAM; DAWE, 2020b) was acquired as a 30 m resolution raster layer and the average burn severity (scale = 0-24) estimated for each site at two spatial scales: (1) within a 20 m buffer surrounding each stream transect, and; (2) within a 100 m buffer of the transect midpoint.
Both were strongly correlated with burn severity measured during site assessments (r > .9 when tested against the scored burn severity of the banks to 20 m).
Two remote-sensed measures of drought-severity were also derived, both of which are spectral indices known to be strongly correlated with water availability for vegetation (Caccamo et al., 2012). The visible atmospherically resistant index (VARI; Gitelson et al., 2002) is sensitive to vegetation greenness, whereas the normalized difference infrared index centered on 1650 nm Lastly, elevation (m asl) of the transect mid-point was estimated from a 5 m resolution digital elevation model from Geosciences Australia. Site elevation is a strong predictor of habitat suitability for both P. kundagungan (Bolitho et al., 2021) and P. richmondensis (Willacy, 2014) and therefore was an important covariate for modeling the effects of drought and fire on these species.

| Data analysis
To assess the proportion of suitable habitat burnt during the fires, we first identified streams potentially occupied by each species using the approach of Bolitho et al. (2021). Potential habitat for each species was defined as sections of these streams rasterized to 90 m × 90 m pixels to capture areas of adjoining forest likely to be utilized by Philoria (measured at up to 85 m from breeding sites for P. frosti; Hollis, 2003). The extent of fire within potential habitat was assessed using the GEEBAM layer, with the aid of the sf package for R version 4.0.2 (R Core Team, 2021).
From the wider pool of site-level variables, we selected 10 for inclusion in the analysis of survey data, guided by previous studies (Bolitho et al., 2021;Willacy, 2014) and visual assessment of relationships between these variables and the frog survey data. The 10 variables were elevation, whether sites were burnt or unburnt (based The same candidate model set was fitted to counts of calling males during each survey using generalized linear mixed models (GLMMs). Counts were assumed to follow a Poisson distribution, with the mean count for each species (λ) modeled as a function of site-and survey-level covariates using a log-linear equation. As for occupancy models, only air temperature was included as a predictor of detection rate at the time of survey. Candidate models were fitted sequentially for both species in R using the lme4 package (Bates et al., 2021), with all models including a site-based random effect to account for repeated counts.
Surveys conducted prior to the 2019/2020 fires were used to assess changes in site occupancy and abundance of calling males, and to assess the role of fire and drought in these dynamics. For Black Summer fires (L. Bolitho and D. Newell, unpublished). These surveys followed the same approach as that undertaken during the 2020/2021 field season (repeat surveys conducted from September to January), allowing for direct comparisons.
Changes in site occupancy were assessed using dynamic occupancy models (MacKenzie et al., 2006) fitted to the data with the aid of the unmarked package in R. Within species, models varied only in their structure for the probability of extinction between survey years (ε), but differed slightly between species due to differences in the available data. For P. kundagungan, we fitted models

| Extent of habitat burnt
The area of potential habitat for P. kundagungan was estimated at 69.5 sq. km, of which 21.1 sq. km (30%) was burnt during the 2019/2020 fires. Of the burnt area, 71% was burnt at low-moderate severity, 27% was burnt at high severity, and 2% was burnt at very high severity (based on GEEBAM classifications). For P. richmondensis, 11.9 sq. km of the 96.8 sq. km of potential habitat was burnt (12%), with 45% of the burnt area experiencing low-moderate severity fire, 42% experiencing high severity fire, and 13% experiencing very high severity fire.

| Site occupancy post-fire
Fire severity among the 14 burnt sites for P. kundagungan was generally low to moderate; however, five sites experienced >90% of the stream bed or banks burnt, with two of these experiencing high se-  Figure 3). Effects of fire appeared in the third, fourth, and fifth top models; however, the effects were weak and these models had considerably less support than the top two models excluding fire effects (ΔAIC >2; Table 1). The survey-level probability of detection declined steeply with increasing air temperature for both P. kundagungan and P. richmondensis (Table 2).

| Abundance of calling males post-fire
Counts of calling males were generally low at sites occupied by P. kundagungan (62% of counts at occupied sites being ≤5 individuals).
However, 10 or more individuals were detected on 11 occasions, with a maximum count of 22 in a single site survey. Maximum counts at the two burnt sites at which P. kundagungan was detected were 4 and 10, while at unburnt sites counts averaged 7 individuals, with a range of 1-22. At the three burnt sites at which P. richmondensis was detected, maximum counts of calling males were 1, 3, and 14, with the latter being at a site that was burnt with very low severity. Counts of P. richmondensis at unburnt sites averaged 5, with a range of 1-14.
Rankings of the candidate models when fitted to the count data for each species were very similar to those for the occupancy models (

F I G U R E 3
Relationships between the probability of site occupancy and both elevation and percentage of stream saturated for Philoria kundagungan and Philoria richmondensis post-fire. Relationships are depicted for burnt and unburnt sites for P. kundagungan, with burn status being a key predictor of occupancy probability for this species. Relationships for elevation and percentage of stream saturated are shown with the other covariate held at its mean. Percent stream saturated is the average value across repeat surveys at a site. Shaded areas are 95% confidence intervals.
excluded it (Table 3) and the 95% confidence interval for the effect overlapping zero (Table 4). While burn status also featured in the top model for P. richmondensis (Table 3), the effect was weakly positive (Table 4)

| DISCUSS ION
Assessing the vulnerability of species to climate change is often completed with the aid of correlative environmental niche models that forecast gradual changes in the climatic niche space. However, the rapidity, extent and spatial pattern of declines will also be driven by amplification of the frequency and severity of climate-related stochastic perturbations (Briscoe et al., 2016;Hoffmann, Cavanough, et al., 2021). Understanding species responses to novel stochastic events should therefore be a focus of climate change vulnerability assessments, facilitating integration of specific climate-induced perturbations into predictive models of response (Mathewson et al., 2017;Morán-Ordóñez et al., 2018). Our research on the effects of Australia's unprecedented "Black Summer" wildfires and the associated drought on two rainforest frogs-P. kundagungan and P. richmondensis-provides an empirical case study, and confirms for these species that deepening droughts, drying of breeding sites, and penetration of wildfires into their fire-sensitive habitat represent important proximate threats from climate change.
Remote-sensed mapping of fire severity suggests some 30% of potential habitat was burnt for P. kundagungan and 12% for P. richmondensis. The majority of affected areas burnt at low to moderate severity for P. kundagungan (71%); however, some 55% of habitat burnt for P. richmondensis experienced high severity fire. While persistence at burnt sites was observed for both species, and relatively high counts of calling males at burnt sites were also observed, important negative effects of fire were evident. Observed occupancy rates were substantially lower in burnt habitat for both P. kundagungan (14% in burnt vs. 68% in unburnt) and P. richmondensis (23% in burnt vs. 54% in unburnt), and there was a clear negative effect of fire on site occupancy and persistence probabilities for P. kundagungan, as well as counts of calling males post-fire. These results

TA B L E 5
The top-ranked dynamic occupancy models for Philoria kundagungan and Philoria richmondensis. Percent stream saturated is the average value across repeat surveys at a site in 2020/2021.  As F I G U R E 5 Relationships between the site-level probability of extinction and colonization and measures of drought and fire stress for Philoria kundagungan and Philoria richmondensis. Only relationships for extinction probability are shown for P. kundagungan, for which the probability of colonization was modeled as a constant. Visible Atmospherically Resistant Index is a remote-sensed spectral index that measures water availability for vegetation (hence, higher values = less drought stress). Percent stream saturated is the average value across repeat surveys at a site in 2020/2021. Shaded areas are 95% confidence intervals.
such, forecast increases in temperature, evaporation and rainfall variability (Steffen, 2009) and reduced moisture availability from cloud-stripping (Laidlaw et al., 2011(Laidlaw et al., , 2022) represent a major threat for these high-elevation species, with no capacity for upslope migration  and western Europe (Cayuela et al., 2016). Ultimately, in the face of unmitigated climate change, montane and/or mesic-adapted amphibians with small geographic ranges face an uncertain future.
Nevertheless, we see several options to inform conservation planning for mesic-adapted species at risk from climate drying and future fire events. First, ongoing monitoring provides fundamental insights into the impacts of severe drought and novel fire events, including the areas of species ranges most at risk from these events, and the ecological, demographic and genetic mechanisms through which impacts occur (see also Potvin et al., 2017;Rowley et al., 2020). Second, ecological experiments focusing on these mechanisms allows construction of models that integrate the effects of drought and fire on demographic trajectories, as well as either mechanistic models in which severe drought and fire weather events can be simulated (e.g., Tolhurst et al., 2008), or statistical models built using remote-sensed data on drought and fire extent (e.g., Collins et al., 2021). Taken together, research initiatives such as these offer the potential to predict the scale of the risk posed by drought and fire, and to make spatial projections of that risk. In turn, high-risk populations and lower-risk refugia across a species' range may be identified, facilitating spatial prioritization of conservation investments such as fire-suppression (high-risk populations), preemptive collections for ex situ conservation (high-risk populations) and intensive control of invasive predators or competitors (lowerrisk refugia).
Long-term conservation planning for P. kundagungan and P. richmondensis would benefit from research initiatives such as those Deepening droughts and novel fires represent a significant threat to P. kundagungan and P. richmondensis, just as they do to many mountain-top and/or mesic-adapted species susceptible to climate change . To conclude, we argue that both short-and long-term management pathways exist to confront these threats, including ongoing monitoring to track responses to these threats, conservation planning that explicitly seeks to prepare for their impact, and targeted conservation actions that ameliorate other threatening processes and increase population resilience. writing -original draft (supporting); writing -review and editing (supporting). Ben C. Scheele: Conceptualization (equal); funding